Punica Granatum L.): Features and Medicinal Properties—A Review

plants Review Punica protopunica Balf., the Forgotten Sister of the Common Pomegranate (Punica granatum L.): Features and Medicinal Properties—A Review José Antonio Guerrero-Solano 1 , Osmar Antonio Jaramillo-Morales 2,* , Tania Jiménez-Cabrera 1, Thania Alejandra Urrutia-Hernández 3, Alejandro Chehue-Romero 1, Elena G. Olvera-Hernández 1 and Mirandeli Bautista 1,* 1 Academic Area of Pharmacy, Institute of Health Sciences, Autonomous University of the State of Hidalgo, San Agustin Tlaxiaca, Hidalgo 42160, Mexico; [email protected] (J.A.G.-S.); [email protected] (T.J.-C.); [email protected] (A.C.-R.); [email protected] (E.G.O.-H.) 2 Department of Nursing and Obstetrics, Division of Life Sciences, University of Guanajuato, Ex Hacienda el Copal Km 9 Irapuato-Silao highway ap 311, Irapuato, Guanajuato 36500, Mexico 3 Academic Area of Food Chemistry, Institute of Basic Sciences and Engineering, Autonomous University of the State of Hidalgo, Pachuca-Tulancingo km 4.5 Carboneras, Pachuca de Soto, Hidalgo 42184, Mexico; [email protected] * Correspondence: [email protected] (O.A.J.-M.); [email protected] (M.B.) Received: 1 September 2020; Accepted: 12 September 2020; Published: 16 September 2020 Abstract: Punica protopunica Balf. is one of only two species housed by the Punica genera. Punica protopunica. Balf., known as Socotran pomegranate, is an endemic, isolated species found only in Socotra archipelago in the northwestern Indian Ocean, and is considered to be the ancestor of pomegranate. This review stems from the fact that in many Punica granatum L. articles, Punica protopunica Balf. is mentioned, but just in an informative way, without mentioning their taxonomic and genetic relationship and their medicinal properties. It is there where the need arises to know more about this forgotten species: “the other pomegranate tree.” A large part of the human population does not know of its existence, since only its “sister” has spread throughout the world. The present review deals with the taxonomy and origin of Punica protopunica Balf., the morphology of the tree, distribution, cultivation, vulnerability, and as well as its relationship with Punica granatum L. It also discusses its uses in traditional medicine, its antioxidant capacity, and the medicinal properties of this forgotten species. Keywords: Punica protopunica Balf.; Punica granatum L.; Punica genera; Lythraceae 1. Introduction Myrtales is an order within the classification of terrestrial green plants (Viridiplantae-Streptophyta) [1,2]. The Lythraceae family (from the order of the Myrtales) is composed of herbs, shrubs and trees that are mainly recognized for their flaky bark, crumpled petals from the bud (when emerging out of the rim of the calyx tube of the sepals), leaves oppositely paired, seeds with multi-layered outer integuments, and the fruit is usually a capsule [1–4]. The Lythraceae family comprises 31 genera including the Punica genera [5]. This is quite surprising as the Punica genera has previously been assigned to the monogenic Punicaceae family [6,7]. However, the results of numerous molecular and morphological investigations revealed the close relationship of the genera Punica with the Lythraceae family [1,8–13]. Previously it was considered a monogenic Punicaceae family that contains only one genera, Punica [14,15]. According to Pliny, the name Punica was given by the Romans, referring to the city of Cartago, in Tunis (Punic, Phoenician, Carthaginian), from where Plants 2020, 9, 1214; doi:10.3390/plants9091214 www.mdpi.com/journal/plants Plants 2020, 9, 1214 2 of 15 the best pomegranate (from Latin “pome” witch means apple and “granate” meaning many seeded) arrived in Europe. The genera Punica contains two species, Punica granatum L. and Punica protopunica Balf., [16]. Initially, Punica granatum L. was known as Malum punicum, the apple of Cartago, but later, Carl Linnaeus (1707–1778) chose the current name, with a specific epithet of granatum, which means granular [6]. On the other hand, Punica protopunica Balf. was first described by the Scottish botanist Isaac Bayley Balfour (1853–1922) during his arboreal and botanical expedition in 1880, and published in the Proceedings of the Royal Society of Edinburgh in 1882 [4,14–16]. P. granatum is native to the region that covers territories from a part of Iran to northern India [17,18]. Wild P. granatum L. types have their natural distribution in central Asia from Iran, Afghanistan, Turkmenistan, to northern India, and this region is considered the center of origin of pomegranate [6]. Later, the pomegranate was distributed to the Mediterranean, East Asia, America and South Africa, and this distribution originated the genetic diversity of the pomegranate [19], on the other hand, P. protopunica Balf. is endemic to the Socotra archipelago (located between the Arabian sea and the Guardafui channel in the Indian Ocean, off the coast of the Horn of Africa) [20]. In this context, the objective of this review was to compile the available information on the P. protopunica Balf. species (morphology, distribution, cultivation, vulnerability, uses), including its antioxidant capacity and the medicinal properties, to make it known and allow a wider use of this forgotten wild species. 2. Results 2.1. Taxonomic Positioning and Distribution P. protopunica Balf. (taxonomic positioning in Table1) is an endemic species, found only in the remote archipelago of Socotra, and is considered as one of the most important endemic species on the archipelago [21,22]. Socotra belongs to the Republic of Yemen, it is located at 12◦19’–12◦42’ N and 53◦18’–54◦32’ E, on the Arabian sea of the Indian Ocean [21,23]. Socotra archipelago, also known as the “Galápagos of the Indian ocean” is a group of four islands, Socotra being the most important and largest one. Socotra archipelago (isolated from the rest of the world) is an island with great biological diversity (approximately 900 plant species, 30% endemic) and it hosts unique fauna and flora [24]. People of Socotra use medicinal plants and it is known that this people has a deep respect for nature and its environment [24]. Socotra was included in 2008 to the select list of World Heritage by the United Nations Educational, Scientific and Cultural Organization (UNESCO) under the criteria of natural site [25]. Additionally, P. protopunica Balf. is considered from an independent evolutionary path (due to isolation from the rest of the world) [26], commonly considered as “the other pomegranate tree”, it is an unknown species worldwide, in contrast to the sacred status granted by the name of its species, protopunica: prototype [27]. Table 1. Taxonomic positioning of Punica protopunica Balf. Classification Denomination Common Name Order Myrtales - Family Lythraceae Loosestrife Subfamily Punicoideae - Genera Punica Pomegranate Species Punica protopunica Wild pomegranate, Socotra pomegranate Adapted from [28,29]. P. protopunica Balf. is distributed in different regions of the island, but mainly grows in the central-western part of Socotra, in humid forest regions, in the Haggeher mountains whose slopes are characterized by being made of granite and having a maximum elevation of 1503 m. It also grows on Diksam, the island’s limestone plateau, which rises precipitously 1520 m above sea level. The total area covered has been calculated to be 1/15 of the total area of Socotra (3796 km2)[27]. Plants 2020, 9, 1214 3 of 15 2.2. Morphology Balfour, the discoverer of P. protopunica Balf., described it as “trees with branches, often thorny; elliptic leaves round sheath, oblique; below the oblong, obtuse flower bracts; obovate petals; joined carpels, horizontal basal tone center spiral. From Socotra, a new species that abounds and grows on the peninsula” [30]. Additionally, Balfour wrote: “In general habit, it is not unlike the pomegranate, but its leaves are larger and coarser, and it wants the delicate character of the foliage of that species. The flowers, too, are somewhat smaller, and their turbinate base is more angular. The fruit is very much less in size” [31]. P. protopunica Balf. has morphological differences compared to P. granatum L.; it has larger, narrower leaves, different foliage, continuous flowering, and smaller, pink (not red) flowers. The fruit of P. protopunica Balf. is round, pommel-shaped, with a maximum diameter of 3 cm and a characteristic yellow-greenish or red-brown color when ripe, is smaller, evergreen, with white seeds and less sweet than Punica granatum L. [20,30–33]. Table2 shows morphological characteristics of the species. Table 2. Morphological characteristics of P. protopunica Balf. Punica protopunica Balf. Morphological Characteristics The tree can reach a height of 2.5 to 4.5 m. It is considered a small tree or shrub, but if it reaches more than 9.14 m it can be classified as a tree, that is, it can be considered as both main forms. There are trees that are General habit wider than they are tall (for example, trees that grow on the slopes rocks of Socotra) and trees taller than they are wide (typical of trees growing on the Socotra limestone plateau.) Generally, the tree is equal in width to height, with an upright shrub appearance. The bark is reddish-brown when the tree is young, but changes to a Bark, branches and trunk grayish hue as it grows older. The branches have thorns. The leaves grow to a length of 3 cm, in pairs on the opposite sides of the stalk, they are perennial, their most common shape is elliptical or oblong, Leaves although there are also circular or oval and obovate leaves (a single branch can have leaves of all the shapes described). Its color is dark green, with a bright tone. The flowers have obovate or oval petals, although they are sometimes heart-shaped. Its color is light pink with glitter and its shape is “trumpet”. Flowers Flowering occurs from December until the summer of the following year.

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